Heart and Vessels (2019) 34:1471–1478 https://doi.org/10.1007/s00380-019-01381-6

ORIGINAL ARTICLE

Cardiac in the presence of chronic internal carotid occlusion

Mario Lescan1 · Volker Steger1 · Mateja Andic1 · Kujtim Veseli1 · Helene Haeberle2 · Tobias Krüger1 · Christian Schlensak1

Received: 30 August 2018 / Accepted: 15 March 2019 / Published online: 23 March 2019 © Springer Japan KK, part of Springer Nature 2019

Abstract The aim was to evaluate the incidence of in the setting of cardiac surgery with or without hemodynamically relevant asymptomatic carotid stenosis contralateral to the occlusion. We designed a historical cohorts study, focused on patients with unilateral totally occluded internal carotid who were referred for any cardiac surgery at our center. Isolated unilateral occlusions were assigned to group 1 (n = 60), and those with a contralateral stenosis grade ≥ 60% were included in group 2 (n = 51). A total of 111 patients operated in our center from 1997 to 2016 were included. Patients in group 2 had an asymptomatic contralateral stenosis with a mean stenosis grade of 71 ± 20%. Simultaneous carotid (CEA) was performed in 22 patients from group 2. The overall mortality was 8/111 (7.2%). Carotid- associated mortality was not observed, whereas an overall stroke incidence of 8/111 (7.2%) was detected. The group-related outcome showed comparable results for mortality (group 1: 4/60 (6.7%) vs. group 2: 4/51 (7.8%); p = 1.0). Regarding stroke incidence, group 2 had a higher incidence of overall (2/60 (3.3%) vs. 6/51 (11.8%); p = 0.14) with more contralateral (0/60 (0%) vs. 2/51 (3.9%); p = 0.209) and ipsilateral strokes (2/60 (3.3%) vs. 4/51 (7.8%); p = 0.411). Stroke rate peaked in patients with simultaneous carotid and cardiac surgery (n = 22; 18.2%; p = 0.048). Performing simultaneous CEA during cardiac surgery in the presence of a contralateral occlusion may promote stroke. Asymptomatic contralateral carotid stenosis is a risk factor for stroke in patients with carotid occlusion prior to cardiac surgery.

Keywords Endarterectomy · Carotid · Carotid stenosis · Stroke · Cardiac surgical procedures

Introduction patients with total internal carotid artery occlusion referred for cardiac surgery is not that well established. Carotid occlusion may lead to cerebrovascular insufciency In the setting of cardiac surgery, the aim of our retrospec- if compensatory collateral pathways do not adequately tive study was to evaluate the outcome in those high-risk replace the anatomic blood supply. patients. Regarding the neurological outcome, the impact In case of unfavorable hemodynamic situations which of the CEA and the relevance of a carotid stenosis on the may occur perioperatively during cardiac surgery, those contralateral side to the occlusion were evaluated. pathways may be insufcient to prevent stroke. Chronic total carotid occlusion increases the occurrence of perioperative stroke during isolated carotid endarterectomy (CEA) [1–3]. Materials and methods However, the risk of perioperative mortality and stroke in This study was approved by our local ethics committee (No. 125/2017BO2). We designed a historical cohort study, * Mario Lescan [email protected]‑tuebingen.de focused on patients with unilateral totally occluded internal carotid arteries who were referred for any cardiac surgery at 1 Department of Thoracic and Cardiovascular Surgery, our center. All patients received a carotid ultrasound prior University Medical Center Tübingen, Hoppe‑Seyler Strasse to the operation. Patients with isolated unilateral occlusions 3, D‑72076 Tübingen, Germany without contralateral carotid stenosis were assigned to group 2 Department of Anesthesiology, University Medical Center 1. Patients with contralateral internal Tübingen, Tübingen, Germany

Vol.:(0123456789)1 3 1472 Heart and Vessels (2019) 34:1471–1478 with a stenosis of 60% or greater were included in group Statistical analysis 2, who were either referred for isolated cardiac surgery or for the synchronous carotid endarterectomy (CEA). Pre- The statistical analysis was performed using the SPSS 23 operative diagnostics for carotid stenosis were performed software (IBM Corporation, Somer, NY, USA). All variables by duplex sonography, and the stenosis grade was assessed were tested for normality using the Kolmogorov–Smirnov according to NASCET-based criteria [4]. test. After Gaussian distribution was proven, two tailed We evaluated the postoperative outcomes such as death, t-tests were used for further evaluation of the metric data. stroke and myocardial infarction. All patients with postop- In terms of nominal variables, the statistical signifcance erative stroke were isolated from the cohort. Subsequently, between the groups was assessed by Fisher’s exact test. In they were analyzed for the severity of stroke according to this work, metric variables are presented as the mean with the NIHSS score in the acute phase as proposed by Kasner the standard deviation in parentheses, whereas ordinal varia- et al. and modifed Rankin scale (mRS) at discharge based bles are shown as percentages. p values < 0.05 were regarded on medical records [5]. Subgroup analysis was performed as statistically signifcant. to evaluate the risk of simultaneous operations in patients with a carotid occlusion. Myocardial infarction, shock or embolism-promoting disease, such as endocarditis, were Results defned as exclusion criteria. From January 1997 to December 2016, a total of 113 patients Data acquisition with a completely occluded internal carotid artery were scheduled for cardiac surgery. One patient with endocardi- tis and another patient in cardiogenic shock were excluded Data acquisition was performed based on medical records. accordingly to the exclusion criteria. Two study groups were Demographic data and the existence of morbidity predictors formed: group 1 (n = 60) with intact contralateral carotid were included. Outcome parameters of the two groups were arteries, including patients with contralateral stenosis grade in-hospital mortality and morbidity variables, including any 0–60% and group 2 (n = 51) with an asymptomatic con- stroke, ipsilateral stroke, contralateral stroke, myocardial tralateral stenosis greater than 60%. The follow-up time was infarction, carotid-related mortality and delirium. Postopera- defned by the duration of the mean hospital stay (in-hospital tive stroke was defned as an acute focal dysfunction of the outcome), which was 15.6 ± 7.8 days in the overall study brain lasting longer than 24 h with an evidence of infarction population (group 1: 16 ± 9 d; group 2: 15 ± 5 d; p = 0.445). in the CT imaging [6]. Elevation of creatine kinase (CK) lev- els with concomitant signifcant elevation of CK-MB levels (both measured 24 h postoperatively) and ST-segment eleva- Baseline characteristics tion in the ECG were indicative of postoperative myocardial infarction [7]. Table 1 shows the characteristics of patients from both study groups. The group profles were similar regarding comor- bidities. Demographically, patients in group 2 were 3.3 years Surgery older (p < 0.05) than in group 1 (Table 1). At the same time, there were more combination procedures in group 2, All surgical procedures were performed under general whereas aortic valve replacement was performed more fre- either in cardioplegic cardiac arrest on cardio- quently in group 1. Isolated CABG was the most common pulmonary bypass (CABG, aortic valve repair and aortic operation (80% of all surgical procedures). CABG without valve repair + CABG) or as of-pump coronary artery bypass (OPCAB) was accomplished in (OPCAB) procedures. Synchronous CEA was accomplished 10% of all cases. The OPCAB rate was before sternotomy in 22 patients from group 2. Routine higher in group 2 (8.3 vs. 12.3%). The mean contralateral carotid shunting was employed to avoid clamping ischemia carotid stenosis level in group 2 was 71 ± 20%. during CEA. Neuromonitoring was assessed by near-infrared spectrometry (INVOS™, Medtronic, Minneapolis, USA) in Overall outcome all procedures. Postoperatively, patients were transferred to the intensive care unit, where neurological examination We report an overall mortality of 7.2%; however, carotid- occurred after extubation. Patients with neurological symp- associated mortality was not observed. Table 2 gives an toms were additively evaluated by neurologists. Native CT overview of the causes of death observed in this study. scans were performed directly after the neurological diag- Stroke occurred in 8.1% of the cases in the entire study nosis and 24 h after symptom onset.

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Table 1 Baseline characteristics Characteristic Group 1 Group 2 p of study groups 1 and 2 n = 60 n = 51

Female sex (%) 16.7 17.6 1.000 Age (years ± SDa) 67.5 (± 8.6) 70.8 (± 7.7) 0.039* Ejection fraction (% ± SD) 48.6 (± 12.7) 52.2 (± 11.8) 0.125 Grade of contralateral carotid stenosis (%) – 71 (± 20) – Vertebrobasilar stenosis (%) 13.3 17.6 0.409 Left main disease > 50% (%) 26.6 35.3 0.602 Coronary 3-vessel disease (%) 75 80.4 0.649 Aortic stenosis (%) 18.3 17.6 1.000 CABGb (%) 80 80.4 1.000 AVRc (%) 6.7 2 3.72 AVR + CABG (%) 13.3 17.6 0.602 Renal replacement therapy (%) 1.7 2.0 1.000

*Statistically signifcant (p < 0.05) a Standard deviation b Coronary artery bypass graft c Aortic valve replacement

Table 2 Analysis of the cause No. Age Group CEAa Cardiac surgery Cause of death of death among the study population 1 58 1 No CABGb Respiratory failure 2 78 1 No CABG Pneumonia, sepsis 3 77 1 No CABG Pneumonia, sepsis 4 77 1 No AVRc Low cardiac output syndrome 5 75 2 No AVR Mediastinitis, sepsis 6 74 2 No CABG (OPCAB)d Hyperkalemia 7 72 2 No CABG + AVR Myocardial infarction, cardiogenic shock 8 70 2 Yes CABG Bowel ischemia, sepsis

a Carotid endarterectomy b Coronary artery bypass graft c Aortic valve replacement d Of-pump coronary artery bypass population. A total of six (6.3%) ipsilateral and two (1.8%) 11.8%; p = 0.140). There were more contralateral and ipsilat- contralateral strokes were observed: two mild, fve moder- eral strokes in group 2 (group 1: 0/3.3%; group 2: 3.9/7.8%; ate and one severe stroke according to the NIHSS score. At p = 0.209/p = 0.411). Mortality was non-signifcantly higher discharge, six patients with mild-to-moderate strokes had in group 2 (7.1% vs. 8.5%; p = 0.547). Carotid-associated a mRS of 3, whereas one patient with moderate stroke and mortality was not observed. Other indicators of postop- a patient with severe stroke had a mRS of 4 and 5, respec- erative morbidity (myocardial infarction and postoperative tively. Postoperative cardiac morbidity detected by the delirium) were comparable in both groups. occurrence of postoperative myocardial infarction was low, Considering only the results for CABG procedures with only two cases 2/111 (1.8%). Postoperative delirium (n = 89), the results are reported in Table 3. The incidence of was found in 21.6% of the study population. any stroke (group 1: 1/48 (2.1%) vs. group 2: 5/41 (12.2%); p = 0.091), ipsilateral stroke (group 1: 2.1%; vs. group 2: Group‑related outcomes 7.3%; p = 0.331) and contralateral stroke (group 1: 0% vs. group 2: 4.9%; p = 0.209) was higher in group 2. There were more postoperative strokes in the group 2 with The incidence of stroke peaked in patients with syn- contralateral carotid stenosis (Fig. 1). Regarding all types chronous CEA. The stroke rate in those patients was 4/22 of strokes, group 1 showed a superior outcome (3.3% vs. (18.2%) and thus significantly higher compared to the

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Fig. 1 Incidence of the in- hospital mortality and morbidity parameters in study groups 1 and 2 as a percentage; * statisti- cally signifcant (p < 0.05)

Table 3 Stroke incidence in the CABG subgroups isolated cardiac surgery 4/89 (4.5%; p = 0.048; Table 4). Group 1 Group 2 p Table 5 shows the same trend for CABG patients with con- n = 48 n = 41 tralateral carotid stenosis. Synchronous CEA was associated with a stroke rate of 20% (4/20), whereas isolated CABG in Any stroke (%) 1/48 (2.1%) 5/41 (12.2%) 0.091 the presence of a contralateral stenosis > 60% had a stroke Ipsilateral (%) 1/48 (2.1%) 3/41 (7.3%) 0.331 incidence of 4.8% (1/21; p = 0.184). Contralateral (%) 0/48 (0%) 2/41 (4.9%) 0.209 Stroke rate among patients with concomitant vertebral Analysis of isolated CABG surgery in study groups 1 and 2 artery stenosis and carotid occlusion was not elevated (5.9%; 1/17; p = 1.0) compared to those with patent vertebral arter- ies, and none of the overall strokes were observed in the Table 4 Stroke incidence in patients with carotid occlusion and vertebrobasilar supply area. simultaneous CEA or isolated cardiac surgery Simultaneous ­CEAa Isolated cardiac p surgery Discussion n = 22 n = 89 The management of patients with carotid occlusion undergo- Any stroke (%) 4/22 (18.2%) 4/89 (4.5%) 0.048 ing cardiac surgery is not well established. Smaller studies Ipsilateral (%) 2/22 (9.1%) 4/89 (4.5%) 0.34 that predominantly included CABG patients showed contro- Contralateral (%) 2/22 (9.1%) 0/89 (0%) 0.038 versial results: either a higher incidence of stroke or similar a Carotid endarterectomy neurological outcomes compared to patients without relevant cerebrovascular diseases (Table 6) [8–12]. Prospective stud- ies have not been reported in the literature. Moreover, the reported data fail to prove the optimum treatment of patients Table 5 Stroke incidence in patients with contralateral carotid steno- with stenosis contralateral to the occlusion. sis and simultaneous CEA + CABG or isolated CABG Study design Simultaneous Isolated CABG p ­CEAa + CABGb n = 20 n = 21 This work is of retrospective character. Consequently, the interpretation of the fndings aims to give insights into the Any stroke (%) 4/20 (20%) 1/21 (4.8%) 0.184 topic and to determine the statistical trends. A greater relia- Ipsilateral (%) 2/20 (10%) 1/21 (4.8%) 0.606 bility can be achieved by prospective randomized trials, even Contralateral (%) 2/20 (10%) 0/21 (0%) 0.232 though the realization of such trials is difcult. In our high- a Carotid endarterectomy volume center, we identifed 111 patients in the last 20 years b Coronary artery bypass graft based on our inclusion criteria. In particular, patients with

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Table 6 Literature overview Author n Mortality n (%) Stroke n (%) Stroke (CEA)a n (%) Cardiac surgery cl-CEAb

Illuminati et al. [16] 61 5 (8.6) 4 (6.5) 2 (100) CABGc Yes Brener et al. [18] 49 Not reported 1 (2.0) Not reported CABG Yes Dashe et al. [19] 44 Not reported 9 (20.5) 3 (42.9) CABG, valve Yes Mickleborough et al. [20] 25 Not reported 2 (8.0) – CABG No Schwartz et al. [21] 22 0 (0) 6 (27.3) 3 (33.3) CABG Yes Furlan and Craciun [17] 22 2 (9.1) 3 (13.6) 3 (13.6) CABG Yes Rizzo et al. [22] 21 Not reported 1 (4.8) – CABG, valve No Abbasi et al. [23] 20 Not reported 3 (20) 3 (15) CABG Yes Perler et al. [24] 15 1 (6.7) 1 (6.7) – CABG, valve No Suematsu et al. [25] 13 3 (23.1) 0 (0) 0 (0) CABG, valve Yes Thanvi and Robinson [26] 11 0 (0) 1 (9.1) 0 (0) CABG Yes Total 303 11/144 (7.6%) 31/303 (10.2%) 14/74 (18.9%)

Studies including more than ten patients with a total carotid occlusion who were undergoing cardiac surgery a Stroke after contralateral carotid endarterectomy b Endarterectomy of the carotid artery contralateral to the occlusion c Coronary artery bypass graft pronounced morbidities, including ongoing myocardial setting of a combination procedure. Furthermore, aortic infarction, shock or embolism-promoting disease, such as stenosis with an opening area < 1.0 cm2 was present in 20 endocarditis, were excluded from the analysis to avoid bias. patients (17.4%). Aortic stenosis and preoperative hemody- The number of included patients was respectable in both namic instability are regarded as risk factors for stroke in groups. However, the analysis of synchronous CEA patients the presence of carotid stenosis. In our study, one stroke in with contralateral occlusion has to be interpreted critically each study group was observed in patients with aortic valve due to the small subgroup size (n = 22). Furthermore, the stenosis. present study is a retrospective analysis, and thus, the use of the NIHSS score and the mRS to determine the stroke severity must be seen as a limitation, although Kasner et al. Mortality reported high reliability and validity of this method [5]. The NIHSS score was calculated only in those patients, who Cardiac surgery patients without concomitant cerebro- were isolated from the cohort due to focal neurological def- vascular disease were reported to have a mortality rate of cits and pathological imaging. Thus, the conservative stroke 1.4–2.7% for CABG procedures and 2.8% for aortic valve defnition including the imaging and neurological symptoms surgery [8–10]. Carotid stenosis had no impact on periop- may lead to an underestimation of the stroke incidence. erative mortality in patients who were referred for cardiac procedures. Illuminati et al. showed a mortality rate of 1% Baseline characteristics in their prospective study of patients with unilateral carotid stenosis who were scheduled for CABG. In the presence of The study groups were comparable in terms of their demo- a carotid occlusion, the reported mortality rates were higher. graphic data and, particularly, their cardiac and neurologic Tunio et al. reported a mortality rate of 8.6%, whereas Kou- comorbidities. A relevant difference between the study gias et al. found an increase in mortality to 9.1%. In our groups was found regarding the age. Higher age was reported study, we observed an overall mortality rate of 7.2%, which to have a negative impact on postoperative morbidity and was comparable to the previous reports, but the diference mortality after cardiac surgery and could have infuenced between the study groups was not statistically signifcant the results of our study [13]. [14, 15]. The elevated mortality rate was induced by other CABG procedures were reported to have better outcomes complications that arose from cardiac surgery rather than regarding stroke incidence rates compared to valve replace- by carotid-related complications (Table 2). The explanation ment or combination procedures [8–10]. In this study, group for higher mortality among patients with carotid occlusion 1 underwent more combination procedures, whereas group may be due to the advanced and comorbidi- 2 underwent more isolated aortic valve repair procedures. ties in these patients. The apparent increased mortality in Only one stroke in each study group was observed in the patients with carotid occlusion observed in our study should

1 3 1476 Heart and Vessels (2019) 34:1471–1478 be considered when selecting patients for surgery that may and a study by Antoniou et al. [1–3] reported a higher stroke be elective in some circumstances. occurrence in patients with contralateral carotid occlusion who were referred for isolated CEA. Those fndings support Stroke the higher overall stroke incidence observed in our study and the poorest outcome in the subgroup of CEA patients. The overall stroke rate in this study was 7.2%, with a bet- Cardiac surgery is frequently associated with the risk of ter neurological outcome in the study group without con- embolization [28]. The main limitation of our study is the tralateral stenosis. The overall stroke rate in our study was lack of evidence to prove that all of the reported strokes were considerably higher than that in CABG procedures with- due to carotid occlusion and not induced by atheroembolism, out carotid stenosis or occlusion [8–10]. Illuminati et al. e.g., from the . To limit that bias, intraoperative epi- described a tendency toward a higher stroke risk of 8.8% in aortic ultrasound, transesophageal echocardiography or CT patients who were referred for cardiac surgery with isolated scans of the aorta may be useful [16, 29]. However, a total unilateral carotid stenosis > 70% [16]. In terms of occlusion, exclusion of that variable is impossible. As an argument in the largest retrospective study so far by Tunio et al. included favor of carotid-associated strokes, we found that strokes 61 patients with carotid occlusion who were scheduled for in patients without CEA always occurred ipsilateral to the CABG.16 This report found a considerable low stroke inci- occlusion. dence of 6.5% when compared to a wide range of reported Bilateral strokes were not observed in our study. In the stroke rates in the literature from 0 to 27.3% (Table 6) [14, CEA subgroup, two strokes occurred on the surgical side 15, 17–25]. Considering series from the literature, that and two strokes that were ipsilateral to the occlusion. As an included more than ten patients, we found 303 patients with explanation, ischemia on the operated side may be induced carotid occlusions who were referred for cardiac surgery. by embolism from the CEA site. The absence of concomi- Among them, 31 cases of postoperative stroke (10.2%) were tant stroke on the side of the occlusion in those two patients reported. CEA was performed in 74 out of 303 included may be explained by well-established leptomeningeal and patients because of a contralateral hemodynamically rele- ophthalmic artery pathways with additional cerebral blood vant stenosis, resulting in an incidence of stroke in 18.9% of fow reserve. Ischemia on the side of the occluded carotid this subgroup. Encouraged by these fndings, our subgroup artery may be due to impaired collateralization during the analysis of patients with hemodynamically relevant stenosis clamping for CEA. contralateral to carotid occlusion is shown in Table 4. We found a stroke incidence of 18.2% among CEA patients com- Alternative pared to 4.5% among isolated cardiac surgery in the presence of carotid occlusion (p = 0.048). Among CEA patients with The European Society for (ESVS) guide- contralateral carotid occlusion, these results are comparable lines recommend staged or synchronous carotid revascu- to the stroke rates reported by Mickleborough et al. (33.3%), larization prior to CABG in asymptomatic carotid stenosis Rizzo et al. (15%) and Kougias et al. (13.6%) [15, 16, 20, ≥ 70% with contralateral occlusion [30]. Since simultane- 22]. To summarize, stenosis contralateral to the occlusion ous contralateral CEA showed a poor neurological outcome increased the risk of stroke in our study, but contralateral in patients with carotid occlusion prior to cardiac surgery CEA had rather negative efects on neurological outcome. in our study, staged CEA combined with local anesthesia Thanvi et al. described pathogenetic factors for stroke in or previous carotid artery stenting (CAS) may be alterna- the aftermath of carotid occlusion: embolism from the proxi- tives in the treatment of those patients. However, at least mal and distal ends of the stumps, hemodynamic factors and in the context of carotid stenosis, Gopaldas et al. found no combined factors [26]. Contralateral carotid circulation via signifcant diference between “staged” and “synchronous” the posterior and anterior communicating artery, leptome- carotid and cardiac surgery in terms of mortality and neu- ningeal collaterals and retrograde fow via the ophthalmic rological events. The authors reported a stroke rate of 3.9% artery are natural pathways of collateralization and may for more than 16,000 synchronously operated patients and a compensate for the chronic carotid occlusion [27]. However, stroke rate of 3.5% for 6000 patients with “staged” procedure hemodynamic compromise may frequently lead to border- [31]. A recent analysis by Nejim et al. found no risk reduc- zone cerebral ischemia. Considering the poor hemodynamic tion by CAS compared to CEA in more than 4000 patients situations that may occur on cardiopulmonary bypass, due to with carotid occlusion and contralateral stenosis outside postoperative arrhythmias or intraoperative exposure during the context of cardiac surgery [32]. The ESVS guidelines OPCAB procedures, the balance of collateralization may be recommend the CAS as an alternative to surgical revascu- afected by cardiac surgery. Additional collateral blood fow larization, whereby the decision process should be based on imbalance may be induced by clamping for contralateral patient characteristics, symptoms, and center’s experience CEA. Subgroup analyses of the NASCET and ECST trials and perioperative platelet strategy [30]. The major challenge

1 3 Heart and Vessels (2019) 34:1471–1478 1477 of CAS before cardiac surgery is shown in the analysis by 6. Sacco RL, Kasner SE, Broderick JP, Caplan LR, Connors JJ, Cule- Paraskevas et al., who recently reported an overall stroke bras A, Elkind MS, George MG, Hamdan AD, Higashida RT, Hoh BL, Janis LS, Kase CS, Kleindorfer DO, Lee JM, Moseley rate of 8% in a meta-analysis of CAS patients with unilateral ME, Peterson ED, Turan TN, Valderrama AL, Vinters HV (2013) carotid stenosis scheduled for cardiac surgery [33]. In the An updated defnition of stroke for the 21st century: a statement studies included in the meta-analysis, bleeding complica- for healthcare professionals from the American heart association/ tions after cardiac surgery were insufciently reported: The American stroke association. Stroke 44:2064–2089 7. Domanski MJ, Mahafey K, Hasselblad V, Brener SJ, Smith PK, highest reported rate of major bleeding with chest reopening Hillis G, Engoren M, Alexander JH, Levy JH, Chaitman BR, was 5.9%. The meta-analysis revealed that the antiplatelet Broderick S, Mack MJ, Pieper KS, Farkouh ME (2011) Asso- therapy strategy in this special setting is still not standard- ciation of myocardial enzyme elevation and survival following ized on the one hand but seems to play an important role for coronary artery bypass graft surgery. JAMA 305:585–591 8. Shroyer AL, Grover FL, Hattler B, Collins JF, Mcdonald GO, the major events and bleeding complications on the other Kozora E, Lucke JC, Baltz JH, Novitzky D (2009) On-pump hand. versus of-pump coronary-artery bypass surgery. N Engl J Med 361:1827–1837 9. 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